Journal of Bryology ISSN: 0373-6687 (Print) 1743-2820 (Online) Journal homepage: https://www.tandfonline.com/loi/yjbr20 Vertical distribution and diversity of epiphytic bryophytes in the Colombian Amazon Laura V. Campos, Sylvia Mota de Oliveira, Juan Carlos Benavides, Jaime Uribe-M. & Hans ter Steege To cite this article: Laura V. Campos, Sylvia Mota de Oliveira, Juan Carlos Benavides, Jaime Uribe-M. & Hans ter Steege (2019): Vertical distribution and diversity of epiphytic bryophytes in the Colombian Amazon, Journal of Bryology, DOI: 10.1080/03736687.2019.1641898 To link to this article: https://doi.org/10.1080/03736687.2019.1641898 Published online: 05 Sep 2019. Submit your article to this journal View related articles View Crossmark data Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=yjbr20 JOURNAL OF BRYOLOGY https://doi.org/10.1080/03736687.2019.1641898 Vertical distribution and diversity of epiphytic bryophytes in the Colombian Amazon Laura V. Campos Hans ter Steege a b , Sylvia Mota de Oliveira b , Juan Carlos Benavides c , Jaime Uribe-M. d and a Universidad de La Salle, Bogotá, Colombia; bNaturalis Biodiversity Center, Leiden, The Netherlands; cDepartment of Ecology and Territory, Pontificia Universidad Javeriana, Bogotá, Colombia; dInstituto de Ciencias Naturales, Universidad Nacional de Colombia, Avenida carrera 30 # 45-03, edificio 425, Bogotá, Colombia ABSTRACT KEYWORDS Introduction. The purpose of this study was to analyse the variation in the vertical and spatial distribution of epiphytic bryophytes across four forests in the north-western Amazon. We sampled along the entire vertical gradient from tree base to upper canopy in order to answer these questions: Is there vertical zonation? Is there a relationship between composition species and geographical distance? Methods. The vertical gradient was studied in 64 phorophytes, and each phorophyte was divided into six height zones. We used Detrended Corresponded Analysis for plot ordination and Permutation Multivariate Analysis of Variance to analyse variation in species composition. The relationship between species composition and geographic distance was evaluated using a Mantel Test. We used Indicator species analysis to determine the preference of the species for each of the six height zones, and an ANOVA analysis to evaluate the significance of species richness per zone. Key results. There was a gradual differentiation of the bryophyte communities across the tree height zones. We identified 63 indicator species; the tree base had the highest number of indicator species, followed by the outer canopy. Conclusions. The strong influence of height zones on species assemblages revealed the importance of the environmental differences across the vertical gradient within a single tree. Epiphytic bryophyte communities are mainly structured according to the height zone of trees. The presence of a high percentage of indicator species across the Colombian Amazon is evidence to further support a high specificity of species for a particular microhabitat within the forest. Amazon; bryophytes; canopy; Colombia; epiphytes; indicator species; niche assembly; understory; vertical gradient Introduction Bryophytes are a conspicuous component of the epiphytic flora in tropical rainforests (Frahm and Gradstein 1991; Wolf 1993; Acebey et al. 2003), and they are important in terms of ecosystem functioning and species richness (Goffinet and Shaw 2009). Moreover, because of their poikilohydric nature, bryophytes are sensitive indicators of climatic conditions and environmental changes (Vanderpoorten and Goffinet 2009). Bryophyte assemblages show changes in composition and vertical shifts on the host trees when microclimatic conditions change due to deforestation or habitat transformation (Acebey et al. 2003; Frego 2007; Sporn et al. 2010). The distribution of bryophytes vertically up phorophytes in the rainforest can be associated with species-specific preferences to microclimatic conditions (Sporn 2009). The characteristics of the environment change from the bottom of the rainforest upwards into the canopy (Allee 1926); in the canopy, temperatures are higher, and humidity is lower than on the forest floor, limiting the ability of drought-intolerant CONTACT Jaime Uribe-M. © British Bryological Society 2019 Published online 05 Sep 2019 juribem@unal.edu.co species to survive (Kumagai et al. 2001). In this way, some species may grow in a euphotic habitat, in full light (on the outer branches and twigs of the canopy) or under a significant amount of light on exposed branches in the interior but still receiving full sunlight. A different group of species grows in oligophotic habitats, in shady and moist conditions (growing on the lower part of the canopy, trunks, small trees, decaying wood and ground surface). Some species are generalists and can be found in both habitats (Gradstein and Pócs 1989). According to Richards (1984) sun (canopy) and shade (understory) epiphytes are ecological ‘specialists’, while those occurring in almost all height zones are ecological ‘generalists’. An important element in understanding diversity is to understand the factors that determine how species coexist. The coexistence of species in communities has been explained by two mechanisms, niche assembly and dispersal assembly (Mouillot 2007). Both processes can drive community composition, and the relative importance is related to the scale, and the biology of the group being studied (Mota de Oliveira et al. 2009). Following Hubbell (2001), niche assembly 2 L. V. CAMPOS ET AL. assumes that communities are groups of interacting species whose presence or absence is based on the ecological niches or functional roles of the species and that they coexist in interactive equilibrium with other species. In addition, the adaptive equilibrium of member species enables the stability of the community and allows resistance to perturbation. In this type of assembly, the competition for limited resources determines the species composition of the community. On the other hand, dispersal assembly holds that communities are open, species come and go, and their presence or absence is dictated by random dispersal and stochastic local extinction. Dispersal ability is of great importance for plants, that commonly occupy spatially and temporally limited substrate patches (Pohjamo et al. 2006). In general, bryophyte species have broad geographic ranges and are frequently found on more than one continent (Heinrichs et al. 2009). Bryophytes have a tendency to exhibit wider distributions than vascular plants (Vanderpoorten and Goffinet 2009). In bryophytes, a few mechanisms play an important role in dispersal. For instance, rain splash acting on the spores and vegetative gemmae is a mechanism for short-distance dispersal in the understory. Wind, on the contrary, is a mechanism for long-distance dispersal of species growing in the outer canopy. Species growing in exposed areas have a better chance of effective dispersal than species growing in sheltered sites. Because of their small size and low weight, spores are easily picked up and transported by the wind, allowing them to travel several kilometres (Miller and McDaniel 2004; Sundberg et al. 2006). The success of the establishment of dispersed spores, however, also depends on the suitability of the substrate or habitat (Hallingbäck 2002). The geographical distribution of bryophytes is not generally limited by dispersal limitations. Compared to other groups of organisms, bryophytes have relatively low rates of endemism and larger distribution ranges (Patiño and Vanderpoorten 2018). Regarding the dispersion of the species, Lönnell et al. (2014) found that species that have spores up to 25 microns could be dispersed remotely up to 20 km. In addition, as demonstrated by Zanatta et al. (2016), the spores of some bryophytes do not fully comply with Stoke’s law, since the deposition rate of their spores is very low, which helps wind currents to move them away from their place of origin, dispersing propagules across the landscape with a stronger influence of habitat quality and habitat availability than distance to the source (Ross-Davis and Frego 2004). Another factor that must be considered is that the presence and frequency of epiphytic bryophytes is correlated with the connectivity of the trees that are in the same landscape and separated by a few kilometres (Lönnell et al. 2012). Mota de Oliveira and ter Steege (2015) found that, throughout the Brazilian Amazon, the vertical microenvironmental gradient (niche assembly) was the main driver of species composition and that a higher canopy yields a stronger gradient. The purpose of this study was to analyse the variation in the vertical and spatial distribution of epiphytic bryophytes across four forests in the north-western Amazon. We studied the variation in the species composition of communities across six vertical zones within trees from the four forests and across three spatial scales: within single trees, among neighbouring trees, and among sites. We aimed to determine the relative influences of the vertical zonation and medium- and large-scale spatial variation in the composition of epiphytic bryophtyes. We explored whether specific species showed a preference for different height zones in the trees. This is the first study to date that includes sampling of complete trees, including the outer canopy across the Colombian Amazon. Materials and methods Study area Fieldwork was carried out in four upland forests in the Colombian Amazon. Upland forest occupies fairly welldrained and non-flooded clayey soils. The upland forest is the dominant forest type, covering ca. 80% of the total area of Amazonia (ter Steege et al. 2000, 2013). Canopy height of upland forest in the four localities of the study varies from 30 to 40 m (Figure 1). The study area covers over 20.000 km2 of Amazonian forests. Precipitation in all sites exceeds 1000 mm yr−1 with average temperatures of 25°C and relative humidity of nearly 100% at all study sites. The study sites are located up to 400 km apart and have some variability in the physical and climatic setting (Table 1). Data collection We sampled 64 full canopy trees on 4 sites in the Colombian Amazon. At each locality we established four plots of 50 × 50 m. Within the plot we selected four mature rainforest trees (Gradstein 1992; Frahm et al. 2003). Thus, the total sample size for each locality was 16 trees (Figure 2). Trees were selected randomly and only bark texture was considered as a selection factor, excluding trees with peeling bark or particular conditions of the bark that developed a specific and different epiphytic bryophyte community. Tree bark has been considered more important in determining the composition of epiphytic communities than phorophyte identity in lichens (Cáceres et al. 2007), vascular epiphytes (Benavides et al. 2011) and bryophytes JOURNAL OF BRYOLOGY 3 Figure 1. Map of the study area, showing the sampling localities (1. Amazonas, 2. Caquetá, 3. Putumayo, 4. Vaupés) in the Colombian Amazon. (Sporn et al. 2010). The epiphytic bryophytes were sampled in 6 stratified height zones, after Cornelissen and ter Steege (1989). The 6 zones were treated as a proxy for the microclimatic gradient found from the base to the top of the forest (Figure 3). We used the static rope technique to climb the trees and sample in the different height zones (Perry 1978; ter Steege and Cornelissen 1988; ter Steege 1998). The bryophyte communities were sampled using four plots 10 cm2 for each height zone. We had 6 aggregate plots for each tree, 96 for each locality, giving a total of 384 plots. Abundance was not used in our research because size variation made it impossible to separate the individuals of each species. Instead, frequency, measured as the number of plots in which each species was found, was used as a proxy for species abundance (Mota de Oliveira and ter Steege 2013). The specimens were processed at the National Colombian Herbarium (COL). Some collections were deposited at the Herbario Amazonico Colombiano (COAH). The nomenclature of bryophytes was based on Frey and Stech (2009), Gradstein and Uribe (2016), and Churchill (2016). Data analysis Detrended Corresponded Analysis (DCA) was used for plot ordination, using the frequency data. The explained variation (R 2) was calculated as the correlation between the matrices of distances in similarity between the plots, calculated as Euclidean distances, and the Euclidean distance between the plots in the ordination space. We correlated the scores of the plots in the first axis of the ordination with their respective height zone, as this was the expected main environmental gradient. In addition, we analysed variation in species composition through Permutation Multivariate Analysis of Variance (PMAV, Anderson 2001) using a Sorensen distance matrix in each locality. We developed the analysis to test whether the Table 1. Site location and characteristics for the four study sites. Site Amazonas Caquetá Putumayo Vaupés Localities Altitude m Latitude Longitude AT MaxT MinT AP Reserva El Zafire La Gamitana Puerto Colombia Macaquiño 123 134 230 190 −3.99 −0.244 −0.608 1.275 −69.892 −72.413 −74.345 −70.1 25.9 26.3 25.2 25.6 31.3 32.0 31.8 31.6 20.1 20.8 20.6 20.6 2832 2891 2893 3384 Note: AT: Annual Temperature°C, MaxT: Max. Temperature, MinT: Min. Temperature, AP: Annual Precipitation mm. Data from Bioclim (Hijmans et al. 2005). 4 L. V. CAMPOS ET AL. Figure 2. Schematic plots of 50 × 50 m per locality showing distances. similarity values among communities differed between the different height zones, using the species in each plot as our response measurement. In each site we had 96 plots from 16 trees and 6 zones. We observed nesting of the trees within the 50 × 50 m plots and we added this information as strata within the randomisation process (Anderson 2001). The relationship between species composition and geographic distance was evaluated using a Mantel Test (Legendre and Legendre 1998). This tests the null hypothesis of no relationship between two (distance) matrices (McCune et al. 2002), and therefore, we could evaluate whether the dispersal assembly is more important that the niche assembly in the conformation of the bryophyte communities along the trunks. All the analyses were conducted in R statistical software and the vegan package (R-Team 2014). Indicator Species Analysis was used to determine the preference of the species for each of the six height zones (Dufrêne and Legendre 1997). The indicator value (IV) weighs the preferences of the species for a particular zone, using the distribution of the relative frequencies. A randomisation procedure tests for the significance of the indicator value obtained for each species. Species were selected as having an indicator value only if the p value was below 0.05 (Dufrêne and Legendre 1997). We calculated the weighted average height zone for all species in the four localities. The height zone of the species was based on the frequency and number of occurrences per zone; the number indicates the mean zone preference. The zone preference was compared among the same species to verify whether those species considered specialist by the indicator species analysis in one locality maintained their preferred zone across the region. An ANOVA analysis was used to evaluate the significance of species richness per zone. Results Species richness The survey of epiphytic bryophytes across the Colombian Amazon (Amazonas, Caquetá, Vaupés and Putumayo departments), using 384 (40 cm2) plots on 64 trees, resulted in 2827 occurrences of bryophytes. There were a total of 160 species of bryophytes (116 liverworts and 44 mosses), (Campos et al. 2015). The bryophyte species identified belonged to 26 families and 64 genera. Species richness analysis of the data set used in the present study indicates that all sites share a common diversity, except for the Putumayo site, which shows a higher number of species due to an influx of Andean species (Campos et al. 2015) (Figure 4). The highest number of species was found in Table 2. Distribution of overall species diversity of mosses and liverworts across the six height zones in the four localities of the Amazonia. Zone Figure 3. Schematic height zones on a full-grown tree. Z1: tree base; Z2: lower trunk; Z3: upper trunk; Z4: inner canopy; Z5: middle canopy; Z6: outer canopy. Lw Mo S R R% IS IF RS Ss 1 53 25 78 526 18 24 9 14 0.58 2 49 28 77 447 15.8 3 1 2 0.52 3 62 24 86 527 18.6 9 1 1 0.52 4 57 20 77 511 18 8 1 4 0.51 5 53 22 75 440 15.5 4 0 4 0.47 6 52 7 59 376 13.3 14 2 9 0.58 Note: Lw: Number of liverworts species, Mo: Number of mosses species, S: Total number of species, R: Number of records, R%: Proportion of records, IS: Number of indicator species, IF: Number of indicator families, RS: Number of restricted species. Ss: Average Sorensen similarity. JOURNAL OF BRYOLOGY 5 Figure 4. Species-accumulation curves for epiphytic bryophytes measured on sixteen host trees (left; note that the curves for Amazonas and Vaupés overlap) and ninety-six plots (right), in each site. the upper trunk zone (Z3) with 86 species, followed by the tree base (Z1) with 78 species, the lower trunk (Z2) and the inner canopy (Z4) with 77 species each, the middle canopy (Z5) with 75, and the outer canopy (Z6) with 59 species (Table 2). In terms of species richness, there were significant differences among the six height zones (F5,378 = 9.1; p < 0.05), (Figure 5). The families with the highest number of records and species were Lejeuneaceae, Calymperaceae and Lepidoziaceae (Table 3). This was found in all of the sites we studied. The Lejeuneaceae showed a unique vertical distribution because the frequency and number of species increased with the height zone (zone 1–6), while in the other families the number of species and records tended to decrease. Vertical distribution We found a gradual differentiation of the bryophyte communities across the tree height zones, with communities from the base of the tree differing from the communities found in the canopy (Figure 6A). The two first DCA axes explained 63% of the total variation in species composition (Table 4). The stratification of the bryophyte communities across the height zones was repeated at each of the four sites Amazonas, Caquetá, Putumayo and Vaupés. We also found that the second axis of the DCA shows a gradual differentiation from Vaupés to Putumayo to Caquetá to Amazonas (Figure 6B). There was a strong correlation between zone and the position of the plot on the first axis of the DCA for the combined data set (r 2 = 0.772, P < 0.001), (Figure 7). The correlation was also significant when each site was analysed separately. Vaupés had the highest correlation among the sites (r 2 = 0.84, P < 0.001), while Putumayo had the lowest (r 2 = 0.74, P < 0.001). The composition of the species at the different height zones was tested with PMAV, using the height zones and localities as factors. The PMAV used the average Sorensen similarity as the response variable. There was significant differences in the species composition among the different sites, using specific contrasts: Amazonas (Fp 5,90 = 6.7, R 2 = 0.27, Pr = 0.001), Caquetá (Fp 5.90 = 7.3, R 2 = 0.28, Pr = 0.001), Putumayo (Fp 5.90 = 5.5, R 2 = 0.23, Pr = 0.001,) and Vaupés (Fp 5.90 = 9.1, R 2 = 0.33, Pr = 0.001). The highest similarity of the height zones among sites was found at the base of the tree (Z3), followed by the upper canopy (Z6), and the lowest was found in the middle canopy (Z5), followed by the inner canopy (Z4) (Table 2). There was a weak effect of distance on the composition of the plots (Figure 8). The results showed a low correlation between distances in species composition and geographical distance analysing all the plots simultaneously (Mantel’s r = 0.23, P < 0.0001) Indicator species analysis (ISA) Figure 5. Boxplot of differences in species richness among the six height zones. We identified 63 indicator species in our study (Appendix Table A1). The tree base (Z1) had the highest number of indicator species, followed by the outer canopy (Z6), the upper trunk (Z3), the inner canopy 6 L. V. CAMPOS ET AL. Table 3. Species richness and frequency for the three most diverse families across the six height zones. Zone 1 Families Lejeuneaceae Calymperaceae Lepidoziaceae Zone 2 Zone 3 Zone 4 Zone 5 Zone 6 R Sp. R Sp. R Sp. R Sp. R Sp. R Sp. 148 90 81 31 12 11 189 74 44 35 13 7 274 63 42 44 11 7 285 46 32 43 10 6 298 18 25 43 3 5 362 3 – 50 3 – Note: R: records per zone and Sp: number of species per zone. A B Figure 6. (A) DCA ordination (species scores) of 160 epiphytic bryophytes species and 384 plots across the Colombian Amazon. The symbols represent the different height zones. (B) DCA ordination of 160 epiphytic bryophytes species and 384 plots across the Colombian Amazon. The symbols represent the locality of the plots, AM: Amazonas, CA: Caquetá, PU: Putumayo, and VA: Vaupés. Figure 7. Correlation for the Colombian Amazon between the DCA1 and the height zones. R 2 = 0.772, P < 0.001. Table 4. Two informative axes from DCA per site, showing the variation in percentage and the correlation coefficient. Eigenvalues DCA1 Variation DCA2 Variation R 2 P < 0.001 Amazonas Caquetá Putumayo Vaupés 0.711 0.716 0.710 0.681 49.6% 39.7% 36.4% 43.2% 0.363 0.385 0.474 0.351 25.3% 21.4% 24.3% 22.3% 0.819 0.790 0.735 0.840 (Z4), the middle canopy (Z5) and the lower trunk (Z2). In the case of indicator families, 13 families were detected; the Z1 had the highest number of families, followed by Z6, Z2, Z3 and Z4 (Table 2), (Appendix Table A2). Of the 160 species registered, 45 (28%) appeared in only one height zone. The base of the trunk zone (Z1) had 18 (44%) species that were indicators of Z1 zone. JOURNAL OF BRYOLOGY 7 Figure 8. Correlation between geographical distance among the trees and species composition similarity, using the Bray-Curtis similarity index among the 384 plots. The species with the highest indicator value for the trunk base height zone were: Calypogeia tenax, Cololejeunea diaphana, Monodactylopsis monodactyla, Plagiochila sp 1, Prionolejeunea mucronata, Symphyogyna brasiliensis, Syrropodon xanthophyllus and Xylolejeunea crenata. The indicator species with a significant association with the outer canopy zone (Z6) were: Cololejeunea cardiocarpa, Colura greig-smithii, C. tenuicornis, Diplasiolejeunea brunnea, D. buckii, Drepanolejeunea sp1. and Verdoornianthus griffinii. The remaining 115 species were found in more than one height zone and had a low and non-significant indicator value. The indicator value (IV) calculated from the indicator species analysis allowed us to separate the species in two groups: understory specialists (18 species), and canopy specialists (12 species), (Appendix Table A1). Discussion The height zone with the highest species richness was the upper trunk (Z3), a zone where branches and trunk converge. It is possible that the high number of species observed is due to the combination of canopy and trunk communities overlapping at the top of the trunk. In the lower part of the tree, the establishment of epiphytic bryophytes may be limited by the reduced light intensity (Sporn et al. 2010). Our results differ from the findings by Mota de Oliveira et al. (2009), where the richness peak was in the inner canopy (Z4). The difference could be related to the type of canopy (more or less closed), specifically, with the leaf area index (LAI) (Mu et al. 2007; Caldararu et al. 2012; Xiao et al. 2014), because this factor changes the environmental conditions inside the forest, especially the availability of light and moisture (Sillett and Antoine 2004). In general, the frequency of epiphytic bryophytes was higher in the inner canopy, the upper trunk and the tree bases. This is similar to the observations in other neotropical rain forests (e.g. Cornelissen and ter Steege 1989). Vertical stratification is related to environmental conditions such as atmospheric humidity, temperature, light intensity, and wind velocity (Barkman 1958; Proctor 1981; Gentry and Dodson 1987; Cornelissen and ter Steege 1989; Cardelús 2007). The vertical stratification observed in the epiphytic bryophytes is probably driven by the specificity of several species to particular forest strata. For example, Cheilolejeunea urubuensis, Cololejeunea cardiocarpa, Colura greig–smithii, C. tenuicornis, Diplasiolejeunea brunnea, D. buckii, Verdoornianthus griffinii, and V. marsupifolious are creeping epiphytic bryophytes mostly found in the upper canopy (sun epiphytes). The creeping growth (xerotolerant life-form) in the canopy is associated with the strategy to retain water and humidity for extended periods after precipitation events (Zotz et al. 2000). In particular, the genera Colura and Diplasolejeunea have unique morphological characteristics that allow them to tolerate the exposure of the canopy. Colura species have extremely modified leaves that form an apical sac. This genus grows exclusively in the canopy, avoiding the shaded forest understory, while Diplasiolejeunea species have extremely imbricate underleaves, providing an additional layer of protection to the lobules (1 to each lateral leaf). This genus can also grow in the forest understory but in a smaller proportion, (Gradstein et al. 2001; Gradstein and da Costa 2003). Sun epiphytes and generalists are adapted to relatively dry habitats and predictably have better survival chances there. They may descend from the high canopy of the primary forest and establish themselves nearer to the ground in gaps (Gradstein and IlkiuBorges 2009). The upper section of the trunk in the 8 L. V. CAMPOS ET AL. rain forest is occupied by shade-tolerant and droughttolerant species, mainly appressed mats of liverworts from the Lejeuneaceae family (Gradstein and Pócs 1989). In our study, these species, including Ceratolejeunea desciscens, Cheilolejeunea holostipa, Drepanolejeunea anoplantha, Lejeunea laetevirens, and Prionolejeunea scaberula, were indicators for this zone. The species diversity of the lower trunk, although lower than the upper and middle sections of the tree, had a number of unique bryophyte families such as Plagiochilaceae, Lejeuneaceae, Fissidentaceae, Leucobryaceae, Calymperaceae and Leucophanaceae. The presence of those families that are normally found in the understory or even exposed soil of the rainforest was possibly allowed by the high degree of humidity in the Colombian Amazon forest (Richards 1954). The sun and understory epiphytes differ in their reproduction strategy and dispersal range. Our findings agree with the fact that the ability to disperse in shade epiphytes is constrained and that short distance dispersal is mainly by vegetative reproduction (Cleavitt 2002; Löbel and Rydin 2009). For example, we found that understory specialists such as Anomoclada portoricensis, Calypogeia laxa, C. tenax, Cyclolejeunea luteola, Mnioloma paralellogramum, Prionolejeunea scaberula, Riccardia amazonica, and Xylolejeunea crenata frequently produced vegetative gemmae and caducous leaves. In the case of sun epiphytes, spore dispersal generally is common, and the species are predominantly monoicous (Gradstein and Ilkiu-Borges 2009). The predominance of monoicous species was supported by our observations, as most of the canopy specialists, such as Cheilolejeunea urubuensis, Cololejeunea cardiocarpa, Colura tenuicornis, Leptolejeunea elliptica, Verdoornianthus griffinii and V. marsupifolious, were indeed monoicous. In general, we found more similarity in the species assemblages of one height zone among different localities than in the different height zones in one locality. The strong influence of height zones on species assemblages reveals the importance of the environmental differences across the vertical gradient within a single tree. In this way the vertical distribution reflects the underlying moisture gradient, where the communities are strongly stratified through the height zones in the forest (McCune 1993). Temperature gradients within forests have also been shown to influence the frequency of epiphytic bryophytes (Sillett and Antoine 2004). Changes in microclimatic conditions for epiphytic bryophytes include decreasing humidity and increasing exposure to desiccating wind with increasing height in the canopy (Campbell and Coxson 2001). Epiphytes have high dispersal ability and, as a consequence, can rapidly colonise available sites that fall within their dispersal range (Nieder et al. 1999). The high similarity in the community composition in the different zones across the localities is explained by the ease of dispersal across localities. Epiphytic bryophytes from the base of the tree showed a higher similarity in their composition among localities. This is because of the presence of species from genera with widespread distribution such as Leucobryum, Leucophanes, Plagiochilla, Sematophyllum, Symphyogyna (Pócs 1982). A possible explanation for this high similarity is that the continuous distribution of the bryophytes from the tree base to the adjacent soil facilitates dispersal. We found a clear separation between species from the tree base and species from the upper canopy, probably explained by the fact that these forest strata correspond to the extremes of a micro-environmental continuous gradient. In the upper canopy the epiphytes are exposed to high temperatures and low levels of humidity due to solar radiation intensity and high wind velocity. In contrast, in the lower part of the tree, the air humidity is higher, and the light penetration is lower (Kessler 2000). The clear separation between zones 1 and 6 in our observations matches the results in a recent study in the Amazon basin (Mota de Oliveira et al. 2009). The higher richness of liverworts compared with mosses in our study has been observed across tropical lowland forests in South America and Asia (Florschützde Waard and Bekker 1987; Cornelissen and ter Steege 1989; Gradstein et al. 2001; Sporn et al. 2010; Mota de Oliveira and ter Steege 2013). This is due to the high percentage of a single family that drives the species richness: the Lejeuneaceae. Several studies have shown that in tropical lowland forests, this family can make up 70% of all liverwort species present (Cornelissen and ter Steege 1989; Zartman 2003; Gradstein 2006). Lejeuneaceae is not only a species rich and very abundant family in the tropical lowland forest, where it is an important component of the cryptogamic flora, but also contributes to the temperate liverwort flora (Gradstein 2006). For this reason, the species from this family are good candidates for inferring the origin of tropical diversity and their contribution to the non-tropical diversity (Wilson et al. 2007). Most of the species from this family are epiphytic and occur on trunks and branches, twigs, or living leaves in the rain forest (Gradstein et al. 2001). In our study, we found an increase in the number of Lejeuneaceae species with the height zone in contrast to other families, this can be related to the fact that this family is highly specialised among the leafy liverworts, and also has a good capacity for long-distance dispersal (Mizutani 1961; Schuster 1983; Heinrichs et al. 2014). The results of the most recent study on the Amazon region (Mota de Oliveira and ter Steege 2013) are consistent with our results concerning the most abundant families and the most common species. In addition, our results are supported by the description of the characteristic flora in the Amazon region with a high JOURNAL OF BRYOLOGY dominance of liverworts (Gradstein et al. 2001). Decay in similarity among communities across the Colombian Amazon was not directly related to geographic distance, probably due to the environmental similarities among all the sites and high dispersal abilities of bryophytes. Similarity among communities was primarily explained by height zones. In conclusion, Amazon epiphytic bryophyte communities are mainly structured according to the height zone of trees. This means that the occurrence of epiphytic bryophytes is more influenced by microenvironmental differences at the local and regional scale. In contrast, dispersal shows very little geographic structure across the Amazon. Acknowledgments The first author would like to express her gratitude to COLCIENCIAS for sponsoring her doctoral study, to IDEA WILD for climbing equipment, to Dairon Cárdenas, Fernando Jaramillo (SINCHI), Cristina Peñuela (El Zafire reserve) and Jorge Contreras (UNAL) for help with the logistics of field work, to Maklin Muñoz for invaluable field assistance and ensuring safe tree climbing and to Bill Carr, Mary Lou Price, and the anonymous reviewers for their careful reading of our manuscript and their many insightful comments and suggestions. We also thank Rob Gradstein for help with the identification of some specimens. Notes on contributors Laura V. Campos is a botanist interested in many aspects of plant ecology. Her current research is mostly on the systematics and ecology of neotropical bryophytes. Sylvia Mota de Oliveira is a botanist interested in Amazonian plant diversity, especially on bryophyte ecology and biogeography and systematics of Myristicaceae Juan Carlos Benavides main research interest lies on understanding the relationship between plant ecology and ecosystem services in tropical landscapes Jaime Uribe-M. is a bryologist interested in ecology and taxonomy of neotropical bryophytes. His work has focused on liverworts, particularly the systematics of the liverwort genus Frullania. Hans ter Steege is a tropical forest community ecologist and interested in processes that generate and maintain tree diversity, with a focus on the Amazon forest. ORCID Laura V. 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SPECIES Cololejeunea cardiocarpa** Colura greig-smithii** Colura tenuicornis** Diplasiolejeunea brunnea** Diplasiolejeunea buckii** Drepanolejeunea sp.** Leptolejeunea elliptica** Metalejeunea cucullata Microlejeunea bullata Pycnolejeunea macroloba Rectolejeunea emarginuliflora** Verdoornianthus griffinii** Verdoornianthus marsupiifolius** Cheilolejeunea urubuensis** Archilejeunea fuscescens Ceratolejeunea confusa Drepanolejeunea araucariae Octoblepharum stramineum Ceratolejeunea coarina Cheilolejeunea aneogyna Cheilolejeunea neblinensis Leptoscyphus porphyrius Octoblepharum pulvinatum Odontoschisma variabile Syrrhopodon fimbriatus Syrrhopodon flexifolius Anomoclada portoricensis* Bazzania aurescens Ceratolejeunea desciscens Cheilolejeunea holostipa Drepanolejeunea anoplantha Lejeunea laetevirens Octoblepharum albidum Prionolejeunea scaberula* Syrrhopodon cryptocarpos Archilejeunea crispistipula Bazzania hookeri Syrrhopodon hornschuchii Trichosteleum papillosum Calypogeia laxa* Calypogeia tenax* Z1 1 3 Z2 Z3 Z4 Z5 1 4 10 21 3 2 28 3 1 15 29 6 12 1 29 2 6 1 1 1 8 2 18 2 3 7 13 5 2 8 8 2 9 6 23 3 15 6 2 7 16 17 7 5 3 12 7 1 20 11 8 13 20 8 4 3 19 14 14 17 3 25 3 18 11 5 3 1 Z6 17 6 3 5 6 4 13 13 35 30 11 13 37 24 37 1 1 37 2 3 1 5 26 19 15 24 21 11 6 5 2 44 7 6 13 2 24 11 12 8 10 4 2 4 7 13 16 2 6 13 1 20 15 1 5 5 12 2 10 1 9 1 N 17 6 3 5 6 4 16 22 52 119 17 13 42 26 162 11 12 14 9 103 44 38 53 64 30 12 3 39 33 36 57 3 90 3 33 47 50 14 6 15 7 WA 6 6 6 6 6 6 5.8 5 5.6 4.4 5.6 6 5.9 5.9 4.3 4.6 4.5 4.9 4.3 3.7 3.8 3.9 3.6 3.4 3.5 3.8 3 2.5 3 3.7 3.5 3 3.2 3 2.8 2.1 3.1 2.4 2.2 1.2 1 IV 0.25 0.09 0.04 0.07 0.09 0.06 0.16 0.12 0.36 0.11 0.11 0.20 0.50 0.34 0.18 0.07 0.04 0.18 0.04 0.10 0.12 0.09 0.17 0.10 0.06 0.04 0.04 0.14 0.09 0.08 0.07 0.04 0.10 0.04 0.15 0.08 0.09 0.05 0.06 0.15 0.10 IS 6 6 6 6 6 6 6 6 6 6 6 6 6 6 5 5 5 5 4 4 4 4 4 4 4 4 3 3 3 3 3 3 3 3 3 2 2 2 2 1 1 (Continued) 12 L. V. CAMPOS ET AL. Table A1. Continued. SPECIES Cololejeunea microscopica Cololejeunea diaphana* Cyclolejeunea luteola* Fissidens steerei Lejeunea boryana Leucobryum martianum Leucophanes molleri Micropterygium leiophyllum Micropterygium trachyphyllum Mnioloma parallelogramum* Monodactylopsis monodactyla* Pilosium chlorophyllum Plagiochila sp.1* Prionolejeunea mucronata* Riccardia amazonica* Sematophyllum subsimplex Symphyogyna brasiliensis* Syrrhopodon leprieurii* Syrrhopodon simmondsii Syrrhopodon xanthophyllus* Telaranea diacantha* Xylolejeunea crenata* Acrolejeunea torulosa Acroporium guianense Acroporium pungens Amblystegium sp. 1 Anoplolejeunea conferta Telaranea pecten Archilejeunea ludoviciana Archilejeunea parviflora Bazzania cuneistipula Bazzania diversicuspis Callicostella pallida Calymperes erosum Calymperes lonchophyllum Calymperes othmeri Calymperes rubiginosum Ceratolejeunea ceratantha Ceratolejeunea cornuta Ceratolejeunea cubensis Ceratolejeunea guianensis Ceratolejeunea laetefusca Ceratolejeunea sp. Cheilolejeunea adnata Cheilolejeunea clausa Cheilolejeunea oncophylla Cheilolejeunea rigidula Cheilolejeunea trifaria Chiloscyphus coadunatus Cololejeunea gracilis Colura cylindrica Colura sagittistipula Cryphaea sp. 1. Cyclolejeunea peruviana Cyrto-hypnum schistocalix Diplasiolejeunea cavifolia Drepanolejeunea crucianella Drepanolejeunea fragilis Drepanolejeunea lichenicola Drepanolejeunea orthophylla Drepanolejeunea palmifolia Fissidens prionodes Frullania apiculata Frullania caulisequa Frullania kunzei Frullanoides liebmanniana Groutiella obtusa Haplolejeunea cucullata Harpalejeunea oxyphylla Harpalejeunea stricta Harpalejeunea tridens Holomitrium arboreum Lejeunea caespitosa Lejeunea flava Lejeunea phyllobola Lejeunea reflexistipula Lejeunea sp.1 Z1 9 3 30 7 9 57 42 17 11 15 12 20 6 3 5 42 5 12 18 4 10 8 2 1 6 7 Z2 8 1 7 32 25 3 3 7 Z3 1 Z4 Z5 3 25 15 1 1 1 11 7 3 1 4 1 1 15 22 29 11 10 9 5 1 2 1 1 1 1 1 1 1 2 3 5 1 5 1 4 8 1 4 9 2 4 11 1 1 2 1 4 19 5 1 3 1 4 2 1 6 7 Z6 1 1 3 1 3 1 2 3 6 4 2 1 1 4 16 8 2 2 1 2 2 6 1 1 5 18 4 4 22 3 4 2 2 3 18 21 9 1 1 1 1 4 18 3 19 1 2 9 1 1 1 2 1 7 1 8 4 2 1 1 1 5 1 1 1 2 1 4 8 6 3 1 1 2 1 1 1 1 1 1 5 5 1 1 2 1 1 1 1 6 2 3 1 3 1 2 1 1 1 1 1 3 2 2 1 1 2 1 2 1 5 3 1 3 1 4 2 1 1 N 11 3 38 9 20 128 89 21 15 22 12 25 6 3 6 120 5 22 35 4 10 8 4 4 2 1 16 2 2 19 19 35 1 7 5 7 2 11 103 30 7 8 2 1 4 14 71 9 2 1 1 22 4 1 1 2 1 11 5 2 22 1 3 5 13 2 4 1 11 6 2 2 1 16 5 2 3 WA 1,6 1 1.2 1.6 1.8 2 1.9 1.2 1.3 1.3 1 1.2 1 1 1.2 2.6 1 1.5 1.9 1 1 1 5.5 3.5 2.5 5 4 1 1.5 2.8 2.9 3.7 1 4.1 1.8 3.4 2.5 2.1 3.9 3.3 4.4 3.3 4 5 4 3.6 4 3.3 1 6 6 3.5 3.8 6 1 3.5 5 4.2 5.2 5.5 2.3 1 4 5.2 4.3 5 3.8 1 3.9 4 2.5 4.5 4 4.1 3 3.5 5.3 IV 0.1 0.04 0.37 0.08 0.06 0.39 0.31 0.21 0.12 0.16 0.18 0.25 0.09 0.04 0.06 0.23 0.07 0.10 0.13 0.06 0.15 0.12 IS 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 (Continued) JOURNAL OF BRYOLOGY 13 Table A1. Continued. SPECIES Lejeunea sp.2 Lejeunea sp.3 Lepidolejeunea involuta Leptolejeunea exocellata Lopholejeunea eulopha Lopholejeunea nigricans Lopholejeunea subfusca Microlejeunea aphanella Microlejeunea epiphylla Micropterygium parvistipulum Micropterygium pterygophyllum Mniomalia viridis Neckeropsis undulata Pictolejeunea picta Pilotrichum bippinatum Plagiochila disticha Plagiochila montagnei Plagiochila subplana Plagiochila sp.2 Prionolejeunea aemula Prionolejeunea denticulata Pycnolejeunea contigua Radula javanica Radula mammosa Rectolejeunea berteroana Rhacopilopsis trinitensis Schlotheimia torquata Sematophyllum subpinnatum Shiffneriolejeunea amazonica Symbiezidium barbiflorum Symbiezidium transversale Syrrhopodon graminicola Syrrhopodon incompletus Syrrhopodon incompletus var. lanceolatus Syrrhopodon ligulatus Syrrhopodon parasiticus Syrrhopodon prolifer Syrrhopodon rigidus Telaranea nematodes Thysananthus amazonicus Vesicularia vesicularis Z1 Z2 3 1 1 Z3 1 Z4 1 Z5 Z6 N 2 1 7 1 4 2 6 1 5 13 7 11 2 1 1 8 20 32 3 1 10 116 1 1 1 4 3 6 2 11 6 1 4 4 19 3 1 2 1 10 2 1 2 1 1 3 1 1 3 2 1 1 2 1 4 1 2 3 2 3 1 3 4 4 2 2 1 1 1 1 4 2 1 3 2 8 1 7 9 1 7 5 2 4 1 7 3 23 3 12 4 19 1 1 1 17 26 19 1 1 2 2 1 3 1 1 1 1 1 1 1 1 4 5 1 1 3 1 3 2 1 3 1 1 2 1 1 5 5 6 1 1 1 1 1 2 1 4 3 2 WA 3.5 6 3 4 3.8 2.5 4.7 2 4.8 2.4 1.7 3.7 1.5 1 2 2.8 2.9 2.6 2.3 5 3.1 3.6 4 3 6 1.5 4 4 5 4.9 3.2 6 2.5 1.3 3.7 2.7 6 2.5 1 4.8 1 IV IS Z1-Z6: Number of occurrences per zone; N: Total number of occurrences per species; WA: Mid-point of zonation for the species as calculated by weighted average for the species; IV: Indicator value for each species to its maximum class (P < 0.05); IS: Zone for which the species is indicative Bold names are the indicator species. (*) Specialist for the understory, (**) specialist for the canopy. Table A2. Zonation of epiphytic bryophyte families in the Colombian Amazon. FAMILY Aneuraceae Calypogeiaceae Fissidentaceae Lepidoziaceae Leucobryaceae Leucophanaceae Plagiochilaceae Sematophyllaceae Stereophyllaceae Calymperaceae Cephaloziaceae Hypnaceae Lejeuneaceae Amblystegiaceae Callicostaceae Cryphaeaceae Dicranaceae Frullaniaceae Lophocoleaceae Macromitriaceae Neckeraceae Phyllodrepaniaceae Radulaceae Thuidiaceae Z1 5 34 8 81 64 42 20 42 20 48 4 153 1 2 1 1 Z2 1 10 1 44 62 25 16 22 4 49 13 2 189 42 63 15 15 28 1 48 23 274 1 1 1 3 1 1 2 Z3 Z4 Z5 Z6 1 25 39 1 5 13 1 2 39 21 18 10 3 285 298 1 32 56 7 12 31 4 8 2 1 6 15 1 2 1 4 1 2 1 8 12 3 3 362 3 N 6 44 10 224 285 89 69 138 25 205 67 6 1561 1 2 4 2 21 40 7 2 11 2 1 WA 1.2 1.2 1.5 2.4 2.8 1.9 2.6 2.7 1.2 2.7 3.4 1.3 3.9 5 1.5 3.8 4.5 4.5 3.8 3.9 1.5 3.7 3.5 1 IV 0.06 0.35 0.1 0.27 0.2 0.30 0.08 0.19 0.25 0.15 0.10 0.04 0.23 IS 1 1 1 1 1 1 1 1 1 2 3 4 6 Z1-Z6: Number of occurrences per zone; N: Total number of occurrences per species; WA: Mid-point of zonation for the species as calculated by weighted average for the species; IV: Indicator value for each species to its maximum class (P < 0.05); IS: Zone for which the species is indicative. Bold names are the indicator families.